AJR 2001; 177:919-924
© American Roentgen Ray Society
MR Imaging of Pituitary Adenomas After Gamma Knife Stereotactic Radiosurgery
Glenn A. Tung1,
Georg Noren2,
Jeffrey M. Rogg1 and
Ivor M.D. Jackson3
1
Department of Diagnostic Imaging, Brown University School of Medicine, Rhode
Island Hospital, 593 Eddy St., Providence, RI 02903.
2
Department of Neurosurgery, Brown University School of Medicine, Rhode Island
Hospital, Providence, RI 02903.
3
Division of Endocrinology, Department of Medicine, Brown University School of
Medicine, Rhode Island Hospital, Providence, RI 02903.
Received February 13, 2001;
accepted after revision April 3, 2001.
Address correspondence to G. A. Tung.
Abstract
OBJECTIVE. The purpose of this study was to evaluate the response of
pituitary adenomas to radiosurgery as manifested by changes in size and
appearance on serial MR imaging.
MATERIALS AND METHODS. Over a mean follow-up period of 36 months,
changes in 44 pituitary adenomas were assessed on 147 enhanced MR imaging
studies. Prior surgery had been performed in 36 tumors (82%).
RESULTS. At the time of radiosurgery, mean tumor volume was 5.9
± 0.8 cm3 (mean diameter, 2.2 cm). The mean reduction in
volume at last follow-up was 41% (± 5%, p < 0.001), and a
decrease in tumor volume of 25-100% was observed in 34 tumors (77%). Mean
reduction in tumor volume at 6 months after radiosurgery was 9% (p =
0.095); at 1 year, 24% (p < 0.001); at 2 years, 34% (p
< 0.001); at 3 years, 41% (p < 0.001); and at 4 years, 50%
(p = 0.008). Six months after radiosurgery a slight and transient
increase in size was observed in 21% of tumors. During follow-up, neither
decreased contrast enhancement nor cyst development was associated with
changes in tumor volume.
CONCLUSION. Tumor control was observed for most pituitary adenomas
after radiosurgery and occurred gradually over a period of several years. A
small increase in tumor size might be observed in the first 6 months after
radiosurgery. In most cases, reductions in tumor size were not accompanied by
a change in contrast enhancement or cyst formation.
Introduction
Pituitary adenomas are benign tumors originating from cells of the
adenohypophysis. They are the most common neoplasms of the sellar region and
include approximately 8-15% of all intracranial tumors in adults
[1]. The first line of
treatment for secretory pituitary microadenoma is medical therapy or
microsurgery [2,
3]. For many macroadenomas,
surgical removal is the treatment of choice, but a cure is less successful
when there is a large suprasellar component or invasion of local neural or
vascular structures
[3,4,5].
After surgery, radiation therapy is indicated when there has been a failure to
control excess hormone secretion in cases of tumor recurrence, for tumors
extending into the cavernous sinus that are inaccessible to surgery, or as
prophylaxis against recurrence for residual pituitary tumors. Therapeutic
radiation is also used as a primary therapy when a patient refuses surgery or
is a poor candidate for surgery.
Long-term tumor control rates of 77-88% have been reported for pituitary
adenomas treated by conventional fractionated external beam radiotherapy
[3]. The commonly recommended
dose of 45-50 Gy is administered in fractionated doses of 1.5-1.8 Gy over a 5-
to 6- week period. The response of pituitary tumors is often slow, and
complications include hypopituitarism, induction of extrapituitary secondary
malignancy, neuropsychologic adverse effects, and damage to the visual
pathway, cavernous sinus contents, or surrounding brain tissue
[6,
7].
Stereotactic radiosurgery refers to the delivery of a therapeutic dose of
ionizing radiation in a single session to a tissue target that has been
precisely localized by imaging-guided stereotaxis. Gamma knife radiosurgery
delivers convergent collimated beams of ionizing radiation from up to 201
shielded cobalt-60 sources in a hemispheric array, but other forms of
radiation have also been used for radiosurgery, including heavily charged
particles and high-energy X-rays from a linear accelerator. One advantage of
radiosurgery is that its highly conformal dose delivery creates a steep dose
gradient at the margin of the target volume and minimizes untoward radiation
of adjacent normal tissue. A single fraction of 20 Gy administered by
radiosurgery is biologically equivalent to 50-110 Gy of fractionated
radiotherapy [8]. Gamma knife
radiosurgery has an accurate and reliable radiation delivery system, and dose
distribution can be modified easily. Like conventional radiation therapy,
radiosurgery is primarily used as an adjunct to surgery for the treatment of
pituitary macroadenomas. However, the effectiveness of radiosurgery for
controlling the growth—defined as an 18% or greater reduction in tumor
volume—has not been established for large non-functional pituitary
tumors [7,
9,
10].
The introduction of MR imaging revolutionized the clinical effectiveness of
radiosurgery by improving the identification and characterization of target
tissues for treatment and by enhancing the precision of pretreatment planning.
However, its role in assessing the response to radiosurgery in posttreatment
follow-up has not been extensively studied for pituitary adenomas. The purpose
of this study was to investigate serial changes in size and appearance of
pituitary adenomas on enhanced MR imaging after gamma knife radiosurgery.
Materials and Methods
Subjects
The subjects of this study were 44 pituitary adenomas treated by gamma
knife radiosurgery at a single center and for which 147 MR imaging studies
were performed. These MR imaging studies consisted of one initial examination
of each tumor, performed immediately before radiosurgery, and one or more
follow-up examinations; one follow-up examination must have been performed at
least 2 years after radiosurgery. Thirty-six (82%) of 44 tumors had been
previously treated by surgery. These 44 tumors were found in 26 women and 18
men with a mean age 56.5 years (range, 28-78 years). Twenty-two tumors (50%)
were nonsecreting tumors, and 22 (50%) were secretory adenomas, including
eight prolactinomas, eight follicle-stimulating hormone-secreting adenomas,
four growth hormone-secreting microadenomas, and two corticotropin-secreting
adenomas.
Gamma Knife Radiosurgery Dosimetry
The dose plan involved the use of multiple injections (isocenters) to
achieve a highly conformal coverage of the tumor with the lowest possible
exposure of surrounding structures, in particular the optic apparatus. In
general, 50% of the maximal radiation dose was delivered to the periphery of
the tumor (50% isodose line). The doses prescribed to the 50% isodose line
were typically 15-20 Gy for nonsecreting adenomas and 20-25 Gy for secreting
tumors. The maximal dose to any small volume of the optic nerves and chiasm
was 10 Gy. The mean tumor dose was 28.8 ± 2.2 Gy (± standard
error of the mean [SEM]), and the mean percentage of tumor that received at
least 25 Gy was 53.6%; 20 Gy, 68.2%; 15 Gy, 82.6%; and 10 Gy, 95.2%.
MR Imaging Method
On the day of radiosurgery, a stereotactic frame was attached to the
patient's head under local anesthesia. This procedure was followed by
contrast-enhanced MR imaging on a 1.5-T magnet (Vision; Siemens, Erlangen,
Germany) using a standard transmit-receive head coil. MR imaging of the
pituitary included coronal and transaxial T1-weighted spin-echo images before
and after the administration of 0.05 mmol/kg of gadopentetate dimeglumine
(Magnevist; Schering, Berlin, Germany). Parameters for coronal conventional
spin-echo T1-weighted MR imaging included the following: TR range/TE range,
600-800/12-20 msec; section thickness, 2 mm; matrix, 224 x 256; field of
view, 260 mm; and number of acquisitions, 3. Parameters for axial conventional
spin-echo T1-weighted MR imaging were as follows: 600-800/12-20; section
thickness, 2 mm; matrix, 224 x 256; field of view, 260 mm; and number of
acquisitions, 3. After three-dimensional contrast administration,
three-dimensional fast low-angle shot T1-weighted images were also obtained
with the following parameters: TR/TE, 31/6; flip angle, 45°; slab, 52 mm;
effective slice thickness, 1 mm; field of view, 260 mm; number of
acquisitions, 2.
Follow-up MR imaging of the pituitary included coronal and parasagittal
T1-weighted spin-echo images before and after the administration of 0.05
mmol/kg of gadopentetate dimeglumine. Parameters for coronal conventional
spin-echo T1-weighted MR imaging were as follows: TR range/TE range,
400-500/12-20; section thickness, 3 mm; matrix, 256 x 256; field of
view, 160 mm; and number of acquisitions, 2. Parameters for sagittal
conventional spin-echo T1-weighted MR imaging included the following: TR/TE,
500/20; section thickness, 3 mm; matrix, 192 x 256; field of view, 180
mm; and number of acquisitions, 1. Turbo spin-echo T2-weighted MR images of
the brain were acquired with the following parameters: TR
range/TEeff, 5000-6000/128; number of signal acquisitions, 1 or 2;
section thickness, 6 mm; echo train length, 23; matrix, 192 x 256; and
field of view, 230 mm. Axial fluid-attenuated inversion recovery images of the
brain were acquired with TR/TE, 9000/105; inversion time, 2500 msec; section
thickness, 5 mm; intersection gap, 2 mm; matrix, 173 x 230; and field of
view, 230 mm.
Method of Measuring Tumor Volume
Pituitary tumor or pituitary gland size was measured in a blinded manner
from hard-copy coronal and sagittal MR images by a neuroradiologist. If the
tumor margin could be clearly demarcated from the normal pituitary gland,
measurements of the maximal tumor diameter were determined on high-resolution
postcontrast T1-weighted images in the coronal (height and width) and sagittal
(anterior-to-posterior diameter) planes. The total volume was estimated from
the product of 11/6, and the three maximal tumor diameters (height, width, and
anterior-to-posterior diameters)
[9]. If a discrete tumor could
not be identified, the volume of all pituitary tissue (i.e., both the tumor
and compressed residual normal pituitary tissue) was measured. However, in
each case, the particular method of measurement was consistent for initial and
follow-up MR imaging examinations. On follow-up, MR imaging, size, signal
intensity, and contrast-enhancement of the tumor were evaluated. Tumor
extension was evaluated relative to displacement of the optic chiasm,
cavernous sinus, and skull base. Cavernous sinus invasion was present when the
internal carotid artery was encased
[11]. Signal intensity and
contrast-enhancement were evaluated qualitatively and were compared with the
baseline MR imaging examination. Cystic change was defined by foci of
nonenhancement and high-signal-intensity on a T2-weighted image.
Statistical analyses were performed using Stat-View (SAS Institute, Cary,
NC). The two-sided Student's t test was used to compare mean tumor
volumes at the time of radiosurgery and at follow-up. We report both mean
tumor volume and SEM. Values for p equal to or less than 0.05 were
considered to be significant.
Results
Change in Tumor Volume After Gamma Knife Radiosurgery
On the baseline MR imaging examination performed at the time of
radiosurgery, mean tumor volume was 5.9 cm3 (± 0.8, SEM),
which corresponds to a mean tumor diameter of 2.2 cm. The range of tumor
volume was 0.17-20.2 cm3. On the last or most recent follow-up MR
imaging examination, the mean tumor volume was 3.9 cm3 (±
0.6), and the average reduction in tumor volume was 41% (± 5%,
p < 0.0001). Table
1 shows the percentage change in tumor volume on the last
follow-up MR imaging examination compared with tumor volume on the initial
examination. A reduction in tumor volume was observed in 40 cases (91%) and a
decrease in tumor volume of at least 25% was observed in 34 cases (77%). Four
tumors (9%) did not change in size during follow-up.
Mean Tumor Volume at Periodic Follow-Up
The mean follow-up time was 36 ± 1.4 months, and the median
follow-up was 36 months (Fig.
1). In all cases, a follow-up MR imaging examination was performed
2 years or longer after gamma knife radiosurgery, and a mean of 3.3 (range,
1-5) follow-up studies were performed.
Follow-up MR imaging was performed on 34 tumors (77%) at 6 months after
gamma knife radiosurgery and showed a mean tumor volume of 5.8 cm3
(± 0.9). The range of tumor volume was 0.12-18.9 cm3. When
compared with a mean tumor size of 6.4 cm3 (± 1.0) on
initial MR imaging, there was an average decrease in tumor volume of 9%
(± 6%); this change was not statistically significant (p =
0.095). In seven cases (26%), either no change (n = 2) or a slight
increase (n = 7, 21%) in tumor size was observed. In these seven
cases, the mean increase in tumor diameter was 2.0 mm (range, 0.7-3.7 mm). In
one of these cases, the small increase in tumor size was associated with
symptomatic compression of the optic nerve (Fig.
2A,2B).
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Fig. 2A. —68-year-old man with nonsecretory macroadenoma and
symptomatic left optic nerve compression 6 months after radiosurgery. Enhanced
coronal T1-weighted MR image (TR/TE, 800/23) obtained in stereotactic head
frame shows homogeneously enhancing macroadenoma that compresses prechiasmatic
left optic nerve (arrow).
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Fig. 2B. —68-year-old man with nonsecretory macroadenoma and
symptomatic left optic nerve compression 6 months after radiosurgery. Six
months after radiosurgery, patient presented with deterioration of vision and
temporal field cut. Coronal enhanced T1-weighted MR image (433/23) shows
enlargement of upper half of tumor, decreased contrast enhancement, and
increased compression of optic chiasm.
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Follow-up MR imaging was performed on 30 tumors (68%) at 1 year after gamma
knife radiosurgery and showed an average tumor volume of 5.2 cm3
(± 0.8); the range of tumor volumes was 0.5 to 16.4 cm3.
Compared with the initial tumor volume of 6.9 cm3 (± 1.1),
the average reduction in tumor volume was 24% (± 6%); this change was
statistically significant (p < 0.001).
Follow-up MR imaging was performed on 39 tumors (89%) at 2 years after
radiosurgery and showed a mean tumor volume of 4.5 cm3 (±
0.7); the range of tumor volume was 0.02 to 19.2 cm3. Compared with
a tumor volume of 6.6 cm3 (± 0.9) on initial MR imaging, the
average decrease was 34% (± 5%), and this was statistically significant
(p < 0.001)).
Follow-up MR imaging was performed on 30 tumors (68%) at 3 years after
radiosurgery and showed a mean tumor volume of 3.2 cm3
(±0.65); the range of tumor volumes was 0.06 to 14.1 cm3.
Compared with the initial mean tumor volume of 5.2 cm3 (±
0.9), the average decrease in tumor volume was 41% (± 6%), which was
statistically significant (p < 0.001).
Follow-up MR imaging was performed on 13 tumors (30%) at 4 years after
gamma knife radiosurgery and showed a mean tumor volume of 2.8 cm3
(± 1.12). The range of tumor volumes was 0.04 to 14.1 cm3.
Compared with the mean tumor volume of 5.1 cm3 (± 1.5) at
baseline, the average decrease in tumor volume was 50% (± 10%), which
was statistically significant (p = 0.0075).
Other Findings on MR Imaging During Follow-Up
Compared with initial MR imaging, 34 pituitary tumors (77%) showed no or
little change in signal intensity or enhancement pattern on follow-up MR
imaging (Fig.
3A,3B,3C).
In 10 cases (23%) a reduction in contrast enhancement was observed (Fig.
4A,4B,4C,4D),
and in five cases (11%) cystic foci were observed in the tumor on at least one
follow-up examination. In two cases, reduced contrast enhancement in the
center of the tumor was associated with an increase in tumor size at 6 months
follow-up. In one of these cases, follow-up MR imaging at 1 and 2 years showed
decreases in tumor size (Fig.
4A,4B,4C,4D).
Neither reduced enhancement (p = 0.36) nor cyst development
(p = 0.23) was significantly associated with change in tumor size on
follow-up MR imaging. Hemorrhage in the tumor, growth in the cavernous sinus,
and skull base invasion were not observed on follow-up MR imaging.
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Fig. 3A. —65-year-old man with gradual reduction of
follicle-stimulating hormone-secreting macroadenoma after gamma knife
radiosurgery. Coronal T1-weighted MR image (TR/TE, 400/11) in stereotactic
frame shows optic chiasm bowed over convex upper border of macroadenoma, which
has tumor volume of 19.3 cm3.
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Fig. 3B. —65-year-old man with gradual reduction of
follicle-stimulating hormone-secreting macroadenoma after gamma knife
radiosurgery. Follow-up enhanced T1-weighted coronal MR image (500/12)
obtained 1 year after radiosurgery shows 55% reduction in tumor volume.
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Fig. 3C. —65-year-old man with gradual reduction of
follicle-stimulating hormone-secreting macroadenoma after gamma knife
radiosurgery. Enhanced T1-weighted coronal MR image performed 2 years after
radiosurgery shows tumor with concave upper border and volume of 8.1
cm3. There has been no change in contrast enhancement pattern.
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Fig. 4A. —47-year-old man with nonsecretory macroadenoma. Before gamma
knife radiosurgery, enhanced coronal T1-weighted MR image (TR/TE, 600/17)
shows enhancing dumbbell-shaped pituitary tumor that compresses optic chiasm
(arrow).
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Fig. 4B. —47-year-old man with nonsecretory macroadenoma. Six months
after radiosurgery, enhanced T1-weighted MR image (500/20) shows tumor
enlargement. Contrast enhancement is more heterogeneous and is reduced
centrally.
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Fig. 4C. —47-year-old man with nonsecretory macroadenoma. MR image
obtained 1 year after radiosurgery shows 50% reduction in tumor volume, and
adenoma no longer compresses chiasm (arrow). Contrast-enhancement
pattern is more homogeneous.
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Discussion
Therapeutic radiation of pituitary adenomas has been recommended after
subtotal resection of a macroadenoma, after gross total resection with
persistently elevated hormone levels, and for recurrent tumor
[12]. When compared with
smaller tumors, the risk of clinically significant recurrence is higher for
macroadenomas because most can only be partially resected. For hypersecretory
pituitary tumors, the goal of treatment is endocrinologic remission. For
non-secreting adenomas, the goal is control of tumor growth, which has been
defined as a reduction of the original tumor volume by at least 18%
[9,
10]. These two therapeutic
endpoints, control of endocrinopathy and tumor growth, are independent. That
is, tumors that decrease or cease hormone production may or may not change in
size following treatment [13,
14].
Our study supports the effectiveness of gamma knife radiosurgery for
controlling the growth of pituitary adenomas. During a mean follow-up of 36
months, we observed a 41% average reduction of tumor volume, and 77% of tumors
had at least a 25% reduction in volume. These results further support the
positive treatment responses reported by other investigators. Through 25
months of follow-up, Park et al.
[15] report a volume reduction
in 29% of 21 pituitary adenomas treated with gamma knife radiosurgery. At 1-3
years after radiosurgery, Morange-Ramos et al.
[16] reported a 25-100%
reduction in tumor diameter on MR imaging in 37% of 19 tumors. We also report
that there is a cumulative effect of single-session gamma knife radiosurgery
in that its full benefit may not be realized for some years. A gradual
reduction in tumor volume may be explained by the radiobiologic effect of
therapeutic radiation. Ionizing radiation damages DNA, and cell demise may
become apparent only after subsequent cellular division or programmed cell
death [17.] Thus, the
cytotoxic effects of radiation therapy may be manifest over a longer period of
time in slowly growing tumors, such as pituitary adenomas. Other cells may
succumb over time to chronic ischemic effects of radiation vasculopathy.
Therefore, unlike surgery, the salutary effects of radiosurgery may not be
realized fully for years after its completion.
A transient increase in the size of brain tumors and vascular malformations
has been reported from 1 to 18 months after whole-brain radiation therapy or
stereotactic radiosurgery
[18,19,20].
The pathophysiology for this "radiation effect" is not known but
may be blood-brain barrier disruption, increased capillary permeability, or
vasogenic edema [21,
22]. We report a slight
increase in the size of 21% of pituitary tumors on MR imaging performed 6
months after radiosurgery. However, by 1 year of follow-up, most of these
tumors were actually smaller than their size before treatment. A similar
temporal resolution of radiation effect has been reported for low-grade
astrocytoma and brain metastases treated by radiosurgery
[20,
23]. As long as it is not
associated with signs or symptoms of critical neural compression, small
increases in adenoma size that are identified on early follow-up MR imaging
after radiosurgery should be followed clinically because the size is likely a
result of radiation effect and should resolve.
After radiosurgery, some tumors have been reported to develop a more
heterogeneous contrast-enhancement pattern that has been attributed to
vascular injury and ischemia
[20,
24]. For example, transient
loss of contrast enhancement has been observed in 70-84% of vestibular
schwannomas after gamma knife radiosurgery
[24,
25]. Although some pituitary
adenomas in this study showed decreased contrast enhancement on follow-up MR
imaging, most of the pituitary tumors showed no change in contrast enhancement
or in the development of intratumoral cysts or hemorrhage. We could find no
significant correlation between contrast-enhancement pattern and tumor control
after gamma knife radiosurgery.
There are several limitations to this study. First, change in tumor size
for secretory tumors may in part be related to concomitant medical therapy.
However, we noted similar reductions in tumor size after radiosurgery for both
secretory and nonsecretory adenomas. Second, MR imaging was not performed in
all cases at each follow-up period. As a result, different sub-groups were
used to evaluate tumor control at each follow-up period. However, because
there was no statistically significant difference in the mean initial tumor
volume between these sub-groups, we believe that inferences on change in tumor
volume over time are valid. Third, slightly different MR imaging protocols
were used for the initial study and for follow-up examinations because
three-dimensional imaging data from the initial study was used to plan gamma
knife radiosurgery. However, we do not think that these differences in
technique had an impact on evaluations of tumor size, signal intensity, or
contrast enhancement.
In conclusion, we report 25% or greater reduction in tumor volume in 77% of
pituitary adenomas treated with gamma knife radiosurgery and a 41% mean tumor
volume reduction. During the first 6 months after radiosurgery, tumor
reduction may not be significant, and a small increase in tumor size may be
seen. However, beginning at 1 year after radiosurgery and for up to 3 years
thereafter, incremental reductions in tumor volume on annual follow-up MR
imaging were observed. In most cases, reductions in tumor size were not
accompanied by a change in contrast enhancement, cyst formation, or
intratumoral hemorrhage.
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Abstract
Introduction
